Here we report that monkeys raised without exposure to faces did not develop face domains, but did develop domains for other categories and did show normal retinotopic organization, indicating that early face deprivation leads to a highly selective cortical processing deficit. Therefore, experience must be necessary for the formation (or maintenance) of face domains. Gaze tracking revealed that control monkeys looked preferentially at faces, even at ages prior to the emergence of face domains, but face-deprived monkeys did not, indicating that face looking is not innate. A retinotopic organization is present throughout the visual system at birth, so selective early viewing behavior could bias category-specific visual responses toward particular retinotopic representations, thereby leading to domain formation in stereotyped locations in inferotemporal cortex, without requiring category-specific templates or biases. Thus, we propose that environmental importance influences viewing behavior, viewing behavior drives neuronal activity, and neuronal activity sculpts domain formation.
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We thank A. Schapiro and D. Tsao for comments on the manuscript. This work was supported by US National Institutes of Health (NIH) grants R01EY25670 (M.S.L.), R01EY16187 (M.S.L.), F32EY24187 (J.L.V.), and P30EY12196 (M.S.L.), and a William Randolph Hearst Fellowship (M.J.A.). This research was carried out in part at the Athinoula A. Martinos Center for Biomedical Imaging at the Massachusetts General Hospital, using resources provided by the Center for Functional Neuroimaging Technologies, a P41 Biotechnology Resource Grant (P41EB015896) supported by the National Institute of Biomedical Imaging and Bioengineering (NIBIB), NIH, and a NIH Shared Instrumentation Grant (S10RR021110).
The authors declare no competing financial interests.
Integrated supplementary information
The stimuli were single large (~10 degrees across) images of monkey faces, familiar objects, monkey hands, or gloved human hands on a pink-noise background; each image subtended 20 x 20 degrees of visual angle.
(top left) Percent of block time that each monkey spent looking within 5° of the central fixation spot during stimulus-presentation blocks accepted for analysis for each category for each scan session, as indicated; different symbols indicate different monkeys, as in Figure 2c legend. (top right) Averages of all images from each category with 5° radius indicated in white. (bottom) Heat maps showing normalized and smoothed average total gaze time at each location on the screen averaged over accepted blocks for each category for example scan sessions from each monkey; maps are overlain on darkened examples of images from that category. Even for session B6 295, which had the lowest percent fixation, the gaze pattern was similar between categories and to that of other monkeys. Slight differences in centering of gaze are due to differences in calibration between sessions. Monitoring gaze direction in the scanner was less accurate than in the free-viewing situation because of longer eye-to-camera distance and less optimal camera angle.
Percent signal change to faces (red), hands (green), or objects (blue) as a function of ventrolateral to dorsomedial distance along an anatomically defined CIT ROI (upper graphs) or an AIT ROI (lower graphs) extending from the crown of the lower lip of the STS to the upper bank of the STS (dotted outlines on the B5 face map in Figure 2). Shading indicates sem. Data were averaged over all sessions and both hemispheres of all three control monkeys that were scanned multiple times (left) and all three face-deprived monkeys (right). Activations were averaged across the AP dimension of the ROI to give an average response as a function of mediolateral location.
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Arcaro, M., Schade, P., Vincent, J. et al. Seeing faces is necessary for face-domain formation. Nat Neurosci 20, 1404–1412 (2017). https://doi.org/10.1038/nn.4635
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